Discussion

In this study, an overall MRSA prevalence at batch-level of 43.8% was detected from samples from batches of pigs at slaughter, combining all ear/nasal and pooled/individual swab results for each batch.

Samples from sow, or sow and boar, batches were significantly less likely to be MRSA positive when compared to finisher pigs. This may affect comparison with other studies which only sampled finisher pigs, although these only represented 15% of the batch population in this study. This difference may also have resulted in lower prevalence estimates from the abattoirs (A and E) from which sows or sows/boars were sampled. However, other studies have detected no substantial difference in the prevalence of MRSA in finisher pigs and sows, especially when from comparable farm types [Reference Crombé2, Reference Broens11]. The individual sample results, suggest a wide variation in the within-batch prevalence of MRSA, but this analysis used only presumptive positive results (where at least one confirmed MRSA was present in the batch) and a relatively small number of batches, and so was limited and requires further study to validate these findings.

When the results were compared to the relative estimates from a 2013 study in the Netherlands (testing pooled nasal swabs) [Reference Broens11], the results from the presented study indicated a much lower prevalence (26.5%) of MRSA, whereas the Netherlands study detected that 67% of breeding and 71% of finishing herds were positive. Although the same laboratory methods were used, the Dutch study used sampling on farm whereas this study sampled at the abattoir. However, Dutch nasal swab results from slaughtered fattening pigs, also from 2013, indicated that 91/93 (97.8%) were positive for MRSA [8]. Comparison to batch-level prevalence, where nasal samples were collected at stunning, from a slaughterhouse survey in Germany also indicated a greater prevalence than this study, with 71% (56 out of 79 herd batches) detected in Germany [Reference Beneke30].

Previous reviews have suggested that the public health risk from consumption, handling or preparation of foodstuffs contaminated with MRSA is very low [31]. People working in abattoirs are occupationally exposed to MRSA, when it is present in the livestock being slaughtered [Reference Normanno15], and have been shown to have a greater prevalence than the general population, although those working with live pigs have been shown to be at greater risk [Reference Van Cleef32]. The degree of exposure is likely to be dependent on numerous factors including food processing procedures and slaughterhouse hygiene practices, as well as the level of contamination of MRSA on carcases and the susceptibility of workers [33, 34].

No MRSA was detected in the UK pig population from the EFSA baseline study of 2008 [5] and so the results here imply that there was subsequent introduction of MRSA and spread within livestock. However, the baseline study differed greatly from the presented study and because of the limited available data it is difficult to draw formal conclusions. The baseline survey investigated environmental samples from pig herds selected according to the survey criteria, was performed a considerable time before this current study, was a farm-based (rather than abattoir based) study and used a laboratory method which had slight variation from procedures adopted later. National data on MRSA bacteraemia cases in people suggests that the case rate reduced from 2008 to the period of this study (5.6 cases per 100 000 population to 1.5 [35]), which may indicate that any increase in MRSA in pigs was having little effect on the prevalence of symptomatic human cases reporting to health care agencies. However, the detection of MRSA in this study suggests that a national monitoring scheme would be useful in order to provide a standardised methodology from which to detect changes in this prevalence estimate over time.

The analysis of results obtained for batches of pigs slaughtered at different times at each abattoir showed that the predominant occurrence of positive batches was at midday, where most of the batches were sampled and which may have been a busy period for the abattoirs. No accompanying management information was collected from the abattoirs (e.g. cleaning or breaks in throughput) and so little could be inferred on the potential cause of variation in results. A predominant spa-type was detected in each abattoir (apart from abattoir B); the predominant spa-type was generally either t011 or t034, types which are both relatively frequently detected in herd level studies of pigs in Europe [10]. The detection of MRSA in batches of pigs may represent contamination from between batches, from other sources within the abattoir, during transport to the abattoir, or persistence of MRSA in the abattoir after initial introduction, rather than accurately reflecting the status of the farm of origin [Reference Broens11, Reference Bouchami12, Reference Normanno15, Reference Ivbule36]. In abattoir E, which was sampled over 2 days, t011 was present on both days possibly suggesting that batches may have been contaminated at the abattoir, which was acting as a reservoir, although t011 tends to be a frequently detected spa-type of MRSA CC398 in pigs in Europe and repeated introduction is equally possible. However, in abattoir C, there were consistent detections of a less common spa-type (t4838) from batches every hour over a 5-h period. Spa-typing alone does not conclusively resolve whether the occurrence was related to cross-contamination, persistence in the abattoir or reintroduction of a spa-type in different batches of pigs. This highlights a need to further explore this and to assess the effectiveness of cleaning strategies for reducing the cross-contamination of MRSA, potentially using whole-genome sequencing methods to provide further discrimination of isolates of MRSA.

All spa-types detected were those associated with LA-MRSA CC398. A previous study of LA-MRSA CC398 isolates from animals in the UK concluded that there have been multiple independent incursions of LA-MRSA CC398 into the UK, with isolates most closely resembling isolates from Europe [Reference Sharma37]. The routes of dissemination of LA-MRSA to the UK are not clear but it could be speculated from the results of this study that other MRSA clones besides CC398 have either not yet reached the UK pig population or were not detected in our study. This study was not designed to be representative of all English pig herds or abattoirs, and was not designed to investigate the national diversity and occurrence of MRSA.

The main source of variation of MRSA results was found at the abattoir level, with wide variation in the prevalence results shown between the six sampled abattoirs. A German study of five abattoirs also showed variability of results between the plants, with prevalence ranging from 59 to 80% [Reference Tenhagen18]. Other studies have shown that slaughter capacity and hygiene practices may affect MRSA occurrence at slaughter [Reference Ivbule36, Reference Narvaez-Bravo38]. Some of this variance in the results at post-stunning may be related to variability on the source farms or in transport and lairage, but in the study of abattoir G a large difference in detection occurred between lairage and post-stunning within the same batches, which supports an abattoir effect. Of specific interest, was that the samples from abattoir D were negative, which was also negative when followed up with an additional sampling visit collecting samples at three points on the line. The prevalence estimated in this study using pooled nasal samples was 28.1%, which indicates that the samples collected from the 26 batches from abattoir D would have been sufficient to detect at least a single MRSA-positive sample with at least 95% confidence.

In the prevalence part of the study, abattoir D was the only gas stunning plant sampled in the prevalence study but the results from the other gas stunning abattoir (abattoir G) showed similar MRSA results to the sampled electric stunning plants. Given the potential for cross-contamination at abattoirs, the results from abattoir D suggests that all contributing batches were MRSA negative on that day of sampling. At the follow-up visit, samples could not be collected in the lairage at abattoir D which meant it was not possible to confirm the status of the pigs entering the abattoir. Additional samples were collected post-singeing, and these may have been more likely to be negative due to the scalding/singeing process.

The results from the three different sampling locations collected at abattoir G suggest that slaughter processes were effective at reducing contamination before carcases entered the chiller. As few lairage samples were positive but almost all post-stunning samples were positive, this suggests that cross-contamination occurred between these stages. However, the same pigs from each batch were not sampled at each location and it was identified that sampling in the lairage was difficult and may have affected the sensitivity of detection and accuracy of these comparisons. There was also a lack of consistent sampling of each batch, with some variation in the number of samples collected at each point and numbers of swabs per pool. Reducing the number of swabs per pooled sample may have reduced the sensitivity of MRSA detection, although not enough data were available to quantify any effect.

The method of isolation used was that recommended by the EU reference laboratory for antimicrobial resistance at the time the study was instigated. Of the suspect colonies from primary cultures undergoing confirmation, 10.3% were found to be negative. Subsequent modifications to the method have been suggested [Reference Larsen39] to reduce the proportion of false-negative samples and these were recently adopted by the EU reference laboratory [40]. Not all positive cultures were confirmed by molecular testing, which may have introduced bias, although at least one positive sample per batch was confirmed and used for batch prevalence estimation. A higher proportion of nasal sample isolates were subject to confirmatory testing. However, the moderate agreement between nasal and ear skin samples may indicate that any bias would have had little effect. A greater level of agreement (0.7; good agreement) had been indicated between these sample types from a comparative farm study [Reference Agersø22]. However, a similar level of agreement (0.4; moderate) had been shown by a previous abattoir study which assessed individual pigs [Reference Sasaki23], and this may indicate the importance of collecting both sample types from pigs to maximise the ability to detect MRSA at slaughter.

This study indicated that in those abattoirs which were investigated, MRSA was overall detected in 43.8% of batches of pigs at slaughter using sensitive selective culture methods. However, it has highlighted that the occurrence of MRSA was variable, specifically between abattoirs, suggesting that a number of factors may influence the occurrence of MRSA in pigs at slaughter. Detailed further investigation of the factors related to cross-contamination at slaughter and examination of different abattoir management practices may hold the key to managing and controlling the occurrence of MRSA in pigs at slaughter and thereby assist in reducing any associated human occupational exposure.